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Spiroplasma Infection Among Ixodid Ticks Exhibits Species Dependence and Suggests a Vertical Pattern of Transmission

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Spiroplasma Infection Among Ixodid Ticks Exhibits Species Dependence and Suggests a Vertical Pattern of Transmission microorganisms Article Spiroplasma Infection among Ixodid Ticks Exhibits Species Dependence and Suggests a Vertical Pattern of Transmission Shohei Ogata 1, Wessam Mohamed Ahmed Mohamed 1 , Kodai Kusakisako 1,2, May June Thu 1,†, Yongjin Qiu 3 , Mohamed Abdallah Mohamed Moustafa 1,4 , Keita Matsuno 5,6 , Ken Katakura 1, Nariaki Nonaka 1 and Ryo Nakao 1,* 1 Laboratory of Parasitology, Department of Disease Control, Faculty of Veterinary Medicine, Graduate School of Infectious Diseases, Hokkaido University, N 18 W 9, Kita-ku, Sapporo 060-0818, Japan; [email protected] (S.O.); [email protected] (W.M.A.M.); [email protected] (K.K.); [email protected] (M.J.T.); [email protected] (M.A.M.M.); [email protected] (K.K.); [email protected] (N.N.) 2 Laboratory of Veterinary Parasitology, School of Veterinary Medicine, Kitasato University, Towada, Aomori 034-8628, Japan 3 Hokudai Center for Zoonosis Control in Zambia, School of Veterinary Medicine, The University of Zambia, P.O. Box 32379, Lusaka 10101, Zambia; [email protected] 4 Department of Animal Medicine, Faculty of Veterinary Medicine, South Valley University, Qena 83523, Egypt 5 Unit of Risk Analysis and Management, Research Center for Zoonosis Control, Hokkaido University, N 20 W 10, Kita-ku, Sapporo 001-0020, Japan; [email protected] 6 International Collaboration Unit, Research Center for Zoonosis Control, Hokkaido University, N 20 W 10, Kita-ku, Sapporo 001-0020, Japan Citation: Ogata, S.; Mohamed, * Correspondence: [email protected]; Tel.: +81-11-706-5196 W.M.A.; Kusakisako, K.; Thu, M.J.; † Present address: Food Control Section, Department of Food and Drug Administration, Ministry of Health and Sports, Zabu Thiri, Nay Pyi Taw 15011, Myanmar. Qiu, Y.; Moustafa, M.A.M.; Matsuno, K.; Katakura, K.; Nonaka, N.; Nakao, R. Spiroplasma Infection among Ixodid Abstract: Members of the genus Spiroplasma are Gram-positive bacteria without cell walls. Some Ticks Exhibits Species Dependence Spiroplasma species can cause disease in arthropods such as bees, whereas others provide their host and Suggests a Vertical Pattern of with resistance to pathogens. Ticks also harbour Spiroplasma, but their role has not been elucidated yet. Transmission. Microorganisms 2021, 9, Here, the infection status and genetic diversity of Spiroplasma in ticks were investigated using samples 333. https://doi.org/10.3390/ collected from different geographic regions in Japan. A total of 712 ticks were tested for Spiroplasma microorganisms9020333 infection by PCR targeting 16S rDNA, and Spiroplasma species were genetically characterized based on 16S rDNA, ITS, dnaA, and rpoB gene sequences. A total of 109 samples originating from eight Academic Editors: David S. Lindsay tick species were positive for Spiroplasma infection, with infection rates ranging from 0% to 84% and Vittorio Sambri depending on the species. A linear mixed model indicated that tick species was the primary factor Received: 24 December 2020 associated with Spiroplasma infection. Moreover, certain Spiroplasma alleles that are highly adapted to Accepted: 5 February 2021 specific tick species may explain the high infection rates in Ixodes ovatus and Haemaphysalis kitaokai. Published: 8 February 2021 A comparison of the alleles obtained suggests that horizontal transmission between tick species Publisher’s Note: MDPI stays neutral may not be a frequent event. These findings provide clues to understand the transmission cycle of with regard to jurisdictional claims in Spiroplasma species in wild tick populations and their roles in host ticks. published maps and institutional affil- iations. Keywords: Haemaphysalis; Ixodes; Spiroplasma; symbionts; ticks; Japan 1. Introduction Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Members of the genus Spiroplasma are Gram-positive bacteria without cell walls. They This article is an open access article are known as symbionts of arthropods and plants and are classified into three major clades distributed under the terms and based on the 16S ribosomal RNA gene (rDNA) sequence: Ixodetis, Citri-Chrysopicola- conditions of the Creative Commons Mirum (CCM), and Apis [1,2]. Spiroplasma is one of the most common endosymbionts Attribution (CC BY) license (https:// with a wide range of hosts, including insects, arachnids, crustaceans, and plants [3]. It is creativecommons.org/licenses/by/ estimated that 5–10% of insect species harbor this symbiont group [2,4]. 4.0/). Microorganisms 2021, 9, 333. https://doi.org/10.3390/microorganisms9020333 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 333 2 of 17 Spiroplasma has a wide range of fitness effects and transmission strategies [2,5–17]. Some Spiroplasma species affect the sex ratio by inducing male killing in hosts such as flies, butterflies, and ladybird beetles [7–10]. Several Spiroplasma species are known to cause disease in arthropods such as bees and plants [6,17,18]. On the other hand, some flies infected with Spiroplasma can develop resistance to other pathogens [5,10–12]. A wide range of symbiotic relationships involving Spiroplasma have been observed [5,7,8,14–16]. The rapid spread of Spiroplasma infection in fruit fly natural populations has been reported in some areas of North America, and this phenomenon has been confirmed in laboratory settings [19]. This characteristic of Spiroplasma is not only biologically interesting, but also useful for symbiotic control applications among host individuals [20]. Ticks have long been studied, since they transmit a variety of pathogens to humans and animals. Spiroplasma mirum is the first reported tick-associated Spiroplasma, which was obtained from Haemaphysalis leporispalustris in the United States in 1982 during the search for rickettsiae in ticks [21]. Another species, S. ixodetis, was isolated from Ixodes pacificus in the United States in 1981 [22]. Thus far, these two species are the only validated Spiroplasma species detected in ticks. Nevertheless, several alleles or putative new species of Spiroplasma have been found in various tick species such as I. arboricola, I. frontalis, I. ovatus, I. persulcatus, I. ricinus, I. uriae, Dermacentor marginatus, Rhipicephalus annulatus, R. decoloratus, R. geigyi, and R. pusillus [23–30]. In Japan, 46 tick species belonging to seven genera (Amblyomma, Argas, Dermacentor, Rhipicephalus, Haemaphysalis, Ixodes, and Ornithodoros) have been recorded [11,12]. Several tick-borne diseases such as Lyme disease, relapsing fever, Japanese spotted fever, severe fever with thrombocytopenia syndrome, and tick-borne encephalitis are endemic [31]. Taroura et al. first detected Spiroplasma DNA in questing I. ovatus ticks captured in several prefectures [24]. Subsequently, a microbiome study revealed the presence of Spiroplasma in the salivary glands of I. ovatus and I. persulcatus [23]. More recently, several Spiroplasma isolates were obtained by incubating the homogenates of I. monospinosus, I. persulcatus, and H. kitaokai with tick and mosquito cells [32]. These studies collectively indicate that there is a close relationship between Spiroplasma and ticks in Japan; however, no comprehensive studies have been conducted to determine the genetic diversity and prevalence of tick- associated Spiroplasma. The aim of this study was to identify and genetically characterize Spiroplasma in different tick species in Japan. A linear mixed model (LMM) was developed to resolve the correlation among several extrinsic and intrinsic factors associated with Spiroplasma infection in ticks. 2. Materials and Methods 2.1. Sample Collection Ticks were collected by flagging the vegetation during the period of tick activity (between April 2013 and August 2018) at 112 different sampling sites in 19 different prefectures in Japan. The sampling sites were classified into nine geographical blocks: Hokkaido (Hokkaido prefecture), Tohoku (Yamagata and Fukushima prefectures), Kanto (Chiba prefecture), Chubu (Nagano and Shizuoka prefectures), Kinki (Mie, Nara, and Wakayama prefectures), Chugoku (Hiroshima and Shimane prefectures), Shikoku (Kagawa, Ehime, and Kochi prefectures), Kyushu (Nagasaki, Kumamoto, Miyazaki, and Kagoshima prefectures), and Okinawa (Okinawa prefecture). All collected ticks were transferred to Petri dishes and preserved in an incubator at 16 ◦C until use. 2.2. Identification of Tick Species Tick species were identified morphologically under a stereomicroscope according to standard morphological keys [33,34]. A total of 712 adult ticks from four genera were examined in this study. These included two species in the genus Amblyomma (A. geoemydae, n = 3; A. testudinarium, n = 26), one species in the genus Dermacentor (D. taiwanensis, n = 9), 10 species in the genus Haemaphysalis (H. concinna, n = 2; H. cornigera, n = 1; H. flava, n = 65; Microorganisms 2021, 9, 333 3 of 17 H. formosensis, n = 83; H. hystricis, n = 60; H. japonica, n = 20; H. kitaokai, n = 78; H. longicornis, n = 106; H. megaspinosa, n = 66; H. yeni, n = 1), and seven species in the genus Ixodes (I. monospinosus, n = 21; I. nipponensis, n = 3; I. ovatus, n = 80; I. pavlovsky, n = 26; I. persulcatus, n = 55; I. tanuki, n = 1; I. turdus, n = 6). 2.3. DNA Extraction The procedures for DNA extraction from individual ticks have been reported previ- ously [35]. In brief, the surface of tick bodies was individually washed with 70% ethanol and sterilized phosphate-buffered solution (PBS). The whole tick bodies were homogenized
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